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Full Text (12.56Mb) UNIVERZITET U BEOGRADU BIOLOŠKI FAKULTET Neda A. Aničić Metabolizam nepetalaktona u listovima odabranih vrsta roda Nepeta (Lamiaceae) i njegova regulacija tokom dehidratacije doktorska disertacija Beograd, 2020 UNIVERSITY OF BELGRADE FACULTY OF BIOLOGY Neda A. Aničić Metabolism of nepetalactone in leaves of selected species of the genus Nepeta (Lamiaceae) and its regulation during dehydration Doctoral Dissertation Belgrade, 2020 Komisija za odbranu doktorske disertacije Mentori: ________________________________________ dr Dragana Matekalo, naučni saradnik, Univerzitet u Beogradu, Institut za biološka istraživanja „Siniša Stanković” Institut od nacionalnog značaja za Republiku Srbiju ________________________________________ dr Tamara Rakić, vanredni profesor, Univerzitet u Beogradu, Biološki fakultet Članovi komisije: ________________________________________ dr Danijela Mišić, naučni savetnik, Univerzitet u Beogradu, Institut za biološka istraživanja „Siniša Stanković” Institut od nacionalnog značaja za Republiku Srbiju ________________________________________ dr Aneta Sabovljević, vanredni profesor, Univerzitet u Beogradu, Biološki fakultet ________________________________________ dr Boban Anđelković, naučni saradnik, Univerzitet u Beogradu, Hemijski fakultet Datum odbrane: ______________________________ Zahvalnica Eksperimentalni deo doktorske disertacije je urađen u laboratorijama Odeljenja za fiziologiju biljaka Instituta za biološka istraživanja „Siniša Stanković” – Instituta od nacionalnog značaja za Republiku Srbiju. Doktorska teza je urađena u okviru projekta osnovnih istraživanja „Fiziološka, hemijska i molekularna analiza diverziteta retkih i ugroženih biljnih vrsta u cilju ex situ zaštite i produkcije biološki aktivnih jedinjenja”, Ministarstva prosvete, nauke i tehnološkog razvoja Republike Srbije (OI173024). Duboku zahvalnost dugujem dragoj mentorki, dr Dragani Matekalo, na svom znanju koje je podelila sa mnom, na dugim diskusijma, strpljenju i pozitivnoj energiji bez kojih bi ovaj dug put bio mnogo teži. Srdačno se zahvaljujem dragoj mentorki, prof. dr Tamari Rakić, na velikoj podršci i predusretljivosti, kao i na korisnim sugestijama, koji su značajno doprineli u uobličavanju teksta ove disertacije. Beskrajnu zahvalnost dugujem dragoj dr Danijeli Mišić; pre svega na ukazanom poverenju da budem deo njene istraživačke grupe, a zatim i na neizmernoj posvećenosti, entuzijazmu i strpljenju, koje mi je nesebično pružala u svim fazama izrade ove disertacije. Zahvaljujem se dr Bobanu Anđelkoviću na angažovanju u realizaciji NMR analiza i pomoći u tumačenju i prezentovanju rezultata. Veliko hvala i prof. dr Aneti Sabovljević na uloženom trudu i konstruktivnim sugestijama. Posebnu zahvalnost dugujem dragoj dr Marijani Skorić za angažovanje u realizaciji eksperimenata iz ove disertacije, za pomoć oko uobličavanja teksta, ali i na ogromnoj podršci i toplim rečima u svim teškim trenucima. Srdačno se zahvaljujem dr Jasmini Nestorović Živković za angažovanje u realizaciji eksperimenta dehidratacije, ali i za svu pozitivnu energiju i bodrenje. Veliku zahvalnost upućujem dr Mileni Dimitrijević i Jeleni Dumanović na realizaciji GC-MS analiza, kao i dr Urošu Gašiću na tumačenju rezultata UHPLC/LTQ - OrbiTrap MS analize. Hvala i dr Milici Radibratović na realizaciji 3D modelovanja proteina. Zahvaljujem se dr Ani Ćirić na angažovanju u realizaciji eksperimenata iz oblasti antimikrobnog dejstva. Veliko hvala i dr Milanu Dragićeviću za pomoć oko statističke obrade rezultata, kao i za i preneseno znanje. Izuzetnu zahvalnost dugujem dr Ilinki Pećinar na realizaciji Ramanove spektroskopije i svetlosne mikroskopije. Zahvalnost na angažovanju u eksperimenatima iz oblasti imunomodulacijskog dejstva dugujem dr Bojanu Jevtiću. Hvala i dr Jovani Hrustić na ukazanom gostoprimstvu tokom eksperimenata rekombinantne ekspresije u E.coli, kao i dr Milošu Brkušaninu na realizaciji sekvenciranja. Svim kolegama sa Odeljenja za fiziologiju biljaka želim ovom prilikom da se zahvalim na kolegijalnosti i pozitivnoj energiji, a naročito dr Slavici Dmitrović, dr Branislavu Šileru, dr Suzani Živković, dr Tijani Banjanac, dr Jeleni Savić, dr Biljani Filipović i Luki Petroviću. Posebnu zahvalnost dugujem dr Milici Milutinović na „čestitkama” iz Amerike, kao i Jeleni Božunović – mojim „malim i nebitnim” kompanjonima. Hvala svim mojim prijateljima što su bili uz mene tokom ovog dugog perioda. Mojim roditeljima, Andriji i Nadeždi, kao i sestri Andrijani, zahvaljujem se na svoj ljubavi i podršci, koju su mi pružali tokom čitavog života. Njima ovu tezu i posvećujem. Metabolizam nepetalaktona u listovima odabranih vrsta roda Nepeta (Lamiaceae) i njegova regulacija tokom dehidratacije Sažetak Specijalizovani metabolizam roda Nepeta (Lamiaceae) karakteriše monoterpenoidni iridoid nepetalakton (NL), koji se javlja u vidu 4 diastereoizomera sa 7S konfiguracijom. Iako se dosta zna o biološkim aktivnostima NL, nedovoljno je istražen njegov metabolizam, kao i uloga u biljkama. Ova doktorska disertacija po prvi put opisuje mehanizme regulacije biosinteze NL tokom dehidratacije u listovima vrsta Nepeta rtanjensis Diklić & Milojević i N. argolica Bory & Chaub subsp. argolica, koje su adaptirane na kserotermna staništa. Uprkos koordinisanom sniženju ekspresije kandidata 10 gena biosintetskog puta iridoida i redukovanoj metaboličkoj aktivnosti, ove vrste su razvile mehanizme za očuvanje nivoa NL u uslovima vodnog deficita. U ovim mehanizmima značajnu ulogu imaju transkripcioni faktori MYC2 i YABBY5 kao pozitivni regulatori biosinteze NL, snižen intenzitet katabolizma NL, kao i očuvanje morfologije glandularnih trihoma, koji predstavljaju glavno mesto biosinteze i akumulacije NL. Iridoid sintaze, čija je funkcija potvrđena enzimatskim in vitro testovima sa rekombinantim proteinima eksprimiranim u heterologom domaćinu Escherichia coli, eksprimiraju se kako kod N. rtanjensis (NrIS2) i N. sibirica L. (NsIS), koje produkuju NL, tako i kod N. nervosa L. (NnIS) koja se odlikuje odsustvom merljivih količina NL u tkivima. N. nervosa očigledno poseduje biosintetsku platformu za produkciju iridoida, koja je neaktivna, najverovatnije usled „gašenja” ili „stišavanja” funkcije nekog gena uzvodno u biosintetskom putu. Rasvetljavanjem mehanizama regulacije metabolizma NL kod vrsta roda Nepeta date su smernice za buduću primenu metaboličkog inženjeringa u cilju optimizacije proizvodnje NL, dok je N. nervosa izdvojena kao interesantna model vrsta za ova istraživanja. Ključne reči: cis,trans-nepetalaktol, dehidratacija, funkcionalna karakterizacija gena, iridoid sintaza, Nepeta, nepetalakton, polietilen glikol, transkripcioni faktori Naučna oblast: Biologija Uža naučna oblast: Fiziologija biljaka UDK broj: 581.13:582.929.4:547.597(043.3) Metabolism of nepetalactone in leaves of selected species of the genus Nepeta (Lamiaceae) and its regulation during dehydration Abstract The specialized metabolism of the genus Nepeta (Lamiaceae) is distinguished by the monoterpenoid iridoid nepetalactone (NL), which exists in the form of 4 diastereoisomers with a 7S configuration. Although its biological activities are well-studied, the NL metabolism, as well as its role in plants, is not well understood. Results of this doctoral thesis describe the regulatory mechanisms determining NL biosynthesis during dehydration, in leaves of Nepeta rtanjensis Diklić & Milojević and N. argolica Bory & Chaub subsp. argolica, which are adapted to xerothermic habitats. Despite a coordinated decrease in the expression of 10 candidate iridoid-related biosynthetic genes and reduced metabolic activity, these species have developed mechanisms to preserve NL levels under water deficit conditions. These mechanisms include the significant role of MYC2 and YABBY5 transcription factors as positive regulators of NL biosynthesis, reduced intensity of NL catabolism, and preservation of the morphology of glandular trichomes – the major site of NL biosynthesis and accumulation. Iridoid synthases, functionaly characterized by in vitro enzymatic assays using recombinant proteins heterologously expressed in Escherichia coli, are expressed in NL-producing N. rtanjensis (NrIS2) and N. sibirica L. (NsIS), as well as in N. nervosa L. (NnIS), which is characterized by the absence of NL in tissues. N. nervosa probably possesses inactive iridoid biosynthetic platform, most likely due to the "switching off" or "silencing" of some genes upstream in the pathway. Elucidation of the regulatory mechanisms behind NL metabolism in Nepeta, provides the background for future metabolic engineering of NL production, and highlightes N. nervosa as an interesting model species for future studies. Key words: cis,trans-nepetalactol, dehydration, functional characterization of genes, iridoid synthase, Nepeta, nepetalactone, polyethylene glycol, transcription factors Scientific field: Biology Scientific subfield: Plant physiology UDK number: 581.13:582.929.4:547.597(043.3) Lista skraćenica 8HGO – 8-hidroksigeraniol oksidaza A549 – ćelije humanog adenokarcinoma AACT – acetil-CoA acetiltransferaza ABA – apscisinska kiselina ANOVA – analiza varijanse BASTA – komercijalni herbicid sa glufosinat-amonijumom bp – bazni par C32 – ćelije humanog melanoma cDNK – komplementarni lanac DNK CDP-MEP – 4-difosfocitidil-2-C-metil-D-eritritol-2-fosfat cis,cis-NL – cis,cis-nepetalakton cis,trans-NL – cis,trans-nepetalakton CMK – 4-(citidin 5-difosfo)-2-C-metil-D-eritritol kinaza COI1 – transkripcioni faktor Coronatine insensitive 1 COSY – korelaciona spektroskopija CTAB – heksadecil-3-metil-amonijum-bromid
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